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Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation

By Mark S Wilson, Matthew D Taylor, Mary T O'Gorman, Adam Balic, Tom A Barr, Kara Filbey, Stephen M Anderton and Rick M Maizels


Numerous population studies and experimental models suggest that helminth infections can ameliorate immuno-inflammatory disorders such as asthma and autoimmunity. Immunosuppressive cell populations associated with helminth infections include Treg and alternatively-activated macrophages. In previous studies, we showed that both CD4+CD25+ Treg, and CD4– MLN cells from Heligmosomoides polygyus-infected C57BL/6 mice were able to transfer protection against allergic airway inflammation to sensitized but uninfected animals. We now show that CD4–CD19+ MLN B cells from infected, but not naïve, mice are able to transfer a down-modulatory effect on allergy, significantly suppressing airway eosinophilia, IL-5 secretion and pathology following allergen challenge. We further demonstrate that the same cell population can alleviate autoimmune-mediated inflammatory events in the CNS, when transferred to uninfected mice undergoing myelin oligodendrocyte glycoprotein(p35–55)-induced EAE. In both allergic and autoimmune models, reduction of disease was achieved with B cells from helminth-infected IL-10−/− donors, indicating that donor cell-derived IL-10 is not required. Phenotypically, MLN B cells from helminth-infected mice expressed uniformly high levels of CD23, with follicular (B2) cell surface markers. These data expand previous observations and highlight the broad regulatory environment that develops during helminth infections that can abate diverse inflammatory disorders in vivo

Topics: Immunity to Infection
Publisher: WILEY-VCH Verlag
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Provided by: PubMed Central

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  7. (2001). B cell development pathways.
  8. (2003). B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD81T cells: role of TGF-b1.
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  13. (2008). B lymphocytes: how they develop and function. Blood
  14. (1997). CD23 deficient mice develop allergic airway hyperresponsiveness following sensitization with ovalbumin.
  15. (2000). CD23 exhibits negative regulatory effects on allergic sensitization and airway hyperresponsiveness.
  16. (2004). CD25 regulatory T cell function.
  17. (2007). CD251regulatory T cells in Heligmosomoides polygyrus infection.
  18. (1994). CD43 (S7) expression identifies peripheral B cell subsets.
  19. (2004). cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development.
  20. (2002). cells control Leishmania major persistence and immunity.
  21. (2002). Chlamydia trachomatis infection inhibits airway eosinophilic inflammation induced by ragweed.
  22. (2002). Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity
  23. (2009). Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity
  24. (2000). Decreased atopy in children infected with Schistosoma haematobium : a role for parasiteinduced interleukin-10. Lancet
  25. Deficiency of regulatory B cells increases allergic airway inflammation.
  26. (1993). deficient mice develop chronic enterocolitis. Cell
  27. Distinct roles of CTLA-4 and TGF-
  28. (2009). Early recruitment of natural CD41Foxp31 regulatory T cells by infective larvae determines the outcome of filarial infection.
  29. Expansion and activation of CD4
  30. (1996). Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice.
  31. (2002). Fas ligand-expressing B-1a lymphocytes mediate CD4(1)-T-cell apoptosis during schistosomal infection: induction by interleukin 4 (IL-4) and
  32. (1990). Fc epsilon RII/CD23: the low affinity receptor for IgE.
  33. (2008). Functional analysis of effector and regulatory T cells in a parasitic nematode infection.
  34. (1992). Heligmosomoides polygyrus : a model for chronic gastrointestinal helminthiasis.
  35. (2010). Helminth infection protects mice from anaphylaxis via IL-10-producing B cells.
  36. (2008). Helminth infections associated with multiple sclerosis induce regulatory B cells.
  37. (2004). Helminth parasites: masters of regulation.
  38. (2006). Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness.
  39. (2003). Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization.
  40. (2009). Immunoregulation by microbes and parasites in the control of allergy and autoimmunity, in:
  41. (2002). Immunoregulation of CNS autoimmunity by helminth and mycobacterial infections.
  42. Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma.
  43. (1997). In infection with Schistosoma mansoni, B cells are required for T helper type 2 cell responses but not for granuloma formation.
  44. (2006). Induction of peripheral T cell tolerance by antigenpresenting B cells. II. chronic antigen presentation overrules antigenpresenting B cell activation.
  45. (2005). Induction, exacerbation and inhibition of allergic and autoimmune diseases by infection. Trends Immunol.
  46. (1998). Infection of B-cell-deficient mice by the parasite Schistosoma mansoni: demonstration of the participation of B cells in granuloma modulation.
  47. (1998). Infection of mice with Mycobacterium bovis-Bacillus Calmette-Guerin (BCG) suppresses allergen-induced airway eosinophilia.
  48. Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol.
  49. (1993). Inhibition of T cell and antibody responses to house dust mite allergen by inhalation of the dominant T cell epitope in naı ¨ve and sensitized
  50. (2009). Interactions between helminth parasites and allergy.
  51. (2002). Intestinal nematode infection ameliorates experimental colitis in mice.
  52. (2002). Long-term protective and antigenspecific effect of heat-killed Mycobacterium vaccae in a murine model of allergic pulmonary inflammation.
  53. (1979). Lymphocytes bearing Fc receptors for IgE. II. Induction of Fce-receptor bearing rat lymphocytes by
  54. (2007). Mapping immune response profiles: the emerging scenario from helminth immunology.
  55. (2006). Memory TH2 cells induce alternatively activated macrophages to mediate protection against nematode parasites.
  56. (2005). Modulation of dendritic cell maturation and function by B lymphocytes.
  57. (2006). natural regulatory T cells in dominant self-tolerance and autoimmune disease.
  58. (2008). Not always the bad guys: B cells as regulators of autoimmune pathology.
  59. (2008). Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe
  60. (2006). Primary T cell expansion and differentiation in vivo requires antigen presentation by B cells.
  61. (2007). Protective effect of Schistosoma mansoni infection on allergic asthma depends on intensity and chronicity of infection.
  62. (2007). Protective immune mechanisms in helminth infection.
  63. (2004). Regulation of allergy and autoimmunity in helminth infection.
  64. (2009). Regulation of pathogenesis and immunity in helminth infections.
  65. (2008). Regulatory B cells as inhibitors of immune responses and inflammation.
  66. (2008). Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression.
  67. (2008). Regulatory role of B cells in a murine model of allergic airway disease.
  68. (2006). regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation.
  69. (2007). Regulatory T cells in allergy and asthma. Chest
  70. (2007). Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice.
  71. (2009). Regulatory T cells: a role in the control of helminth driven intestinal pathology and worm
  72. (2005). Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in
  73. (2010). Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD41 &
  74. (2008). Resting B cells expand a CD41CD251Foxp31Treg population via TGF-beta3.
  75. (2003). Role of regulatory T cells in allergy and
  76. Role of T cell TGF-beta signaling in intestinal cytokine responses and helminthic immune modulation.
  77. (2004). Selective maturation of dendritic cells by Nippostrongylus brasiliensis secreted proteins drives T helper type 2 immune responses.
  78. (2005). Suppression of allergic airway inflammation by helminthinduced regulatory T cells.
  79. (2007). Suppression of Th2-type allergic reactions by helminth infection.
  80. (2006). T cell hyporesponsiveness at sites peripheral to filarial infection.
  81. (1998). T cell-mediated granulomatous pathology in schistosomiasis is downregulated by B cell-dependent mechanism requiring Fc receptor signaling.
  82. (1994). Th2 cells: help for helminths.
  83. (2001). Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol.
  84. (2009). The broader implications of the hygiene hypothesis. Immunology
  85. (2005). The development of IL-4-producing B cells (B effector 2 cells) is controlled by IL-4, IL-4 receptor alpha, and Th2 cells.
  86. (2002). The effect of infections on susceptibility to autoimmune and allergic
  87. (1998). The expression of murine B cell CD23, in vivo, is regulated by its ligand,
  88. (2001). The germless theory of allergic disease: revisiting the hygiene hypothesis.
  89. (2005). The hygiene hypothesis and multiple sclerosis.
  90. (2006). The regulation of allergy and asthma.
  91. The role of CD23 on allergen-induced IgE levels, pulmonary eosinophilia and bronchial hyperresponsiveness in mice.
  92. (2005). TLR ligands can activate dendritic cells to provide a MyD88-dependent negative signal for Th2 cell development.
  93. (2007). TLR-mediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells.
  94. (2002). Tracking the immunoregulatory mechanisms active during allograft tolerance.